The vulnerability of World Heritage seagrass habitats to climate change.

Seagrass is an important natural attribute of 28 World Heritage (WH) properties. These WH seagrass habitats provide a wide range of services to adjacent ecosystems and human communities, and are one of the largest natural carbon sinks on the planet. Climate change is considered the greatest and fastest-growing threat to natural WH properties and evidence of climate-related impacts on seagrass habitats has been growing. The main objective of this study was to assess the vulnerability of WH seagrass habitats to location-specific key climate stressors. Quantitative surveys of seagrass experts and site managers were used to assess exposure, sensitivity and adaptive capacity of WH seagrass habitats to climate stressors, following the Climate Vulnerability Index approach. Over half of WH seagrass habitats have high vulnerability to climate change, mainly from the long-term increase in sea-surface temperature and short-term marine heatwaves. Potential impacts from climate change and certainty scores associated with them were higher than reported by a similar survey-based study from 10 years prior, indicating a shift in stakeholder perspectives during the past decade. Additionally, seagrass experts' opinions on the cumulative impacts of climate and direct-anthropogenic stressors revealed that high temperature in combination with high suspended sediments, eutrophication and hypoxia is likely to provoke a synergistic cumulative (negative) impact (p < .05). A key component contributing to the high vulnerability assessments was the low adaptive capacity; however, discrepancies between adaptive capacity scores and qualitative responses suggest that managers of WH seagrass habitats might not be adequately equipped to respond to climate change impacts. This thematic assessment provides valuable information to help prioritize conservation actions, monitoring activities and research in WH seagrass habitats. It also demonstrates the utility of a systematic framework to evaluate the vulnerability of thematic groups of protected areas that share a specific attribute.

Quantifying blue carbon stocks and the role of protected areas to conserve coastal wetlands.

Vegetated coastal ecosystems, in particular mangroves, tidal marshes and seagrasses are highly efficient at sequestering and storing carbon, making them valuable assets for climate change mitigation and adaptation. The state of Queensland, in northeastern Australia, contains almost half of the total area of these blue carbon ecosystems in the country, yet there are few detailed regional or state-wide assessments of their total sedimentary organic carbon (SOC) stocks. We compiled existing SOC data and used boosted regression tree models to evaluate the influence of environmental variables in explaining the variability in SOC stocks, and to produce spatially explicit blue carbon estimates. The final models explained 75 % (for mangroves and tidal marshes) and 65 % (for seagrasses) of the variability in SOC stocks. Total SOC stocks in the state of Queensland were estimated at 569 ± 98 Tg C (173 ± 32 Tg C, 232 ± 50 Tg C, and 164 ± 16 Tg C from mangroves, tidal marshes and seagrasses, respectively). Regional predictions for each of Queensland's eleven Natural Resource Management regions revealed that 60 % of the state's SOC stocks occurred within three regions (Cape York, Torres Strait and Southern Gulf Natural Resource Management regions) due to a combination of high values of SOC stocks and large areas of coastal wetlands. Protected areas in Queensland play an important role in conserving SOC assets in Queensland's coastal wetlands. For example, ~19 Tg C within terrestrial protected areas, ~27 Tg C within marine protected areas and ~ 40 Tg C within areas of matters of State Environmental Significance. Using multi-decadal (1987-2020) mapped distributions of mangroves in Queensland; we found that mangrove area increased by approximately 30,000 ha from 1987 to 2020, which led to temporal fluctuations in mangrove plant and SOC stocks. We estimated that plant stocks decreased from ~45 Tg C in 1987 to ~34.2 Tg C in 2020, while SOC stocks remained relatively constant from ~107.9 Tg C in 1987 to 108.0 Tg C in 2020. Considering the level of current protection, emissions from mangrove deforestation are potentially very low; therefore, representing minor opportunities for mangrove blue carbon projects in the region. Our study provides much needed information on current trends in carbon stocks and their conservation in Queensland's coastal wetlands, while also contributing to guide future management actions, including blue carbon restoration projects.

A report card approach to describe temporal and spatial trends in parameters for coastal seagrass habitats.

Report cards that are designed to monitor environmental trends have the potential to provide a powerful communication tool because they are easy to understand and accessible to the general public, scientists, managers and policy makers. Given this functionality, they are increasingly popular in marine ecosystem reporting. We describe a report card method for seagrass that incorporates spatial and temporal variability in three metrics-meadow area, species and biomass-developed using long-term (greater than 10 years) monitoring data. This framework summarises large amounts of spatially and temporally complex data to give a numeric score that provides reliable comparisons of seagrass condition in both persistent and naturally variable meadows. We provide an example of how this is applied to seagrass meadows in an industrial port in the Great Barrier Reef World Heritage Area of north-eastern Australia.

Community-specific "desired" states for seagrasses through cycles of loss and recovery.

Seagrass habitats provide critical ecosystem services, yet there is ongoing concern over mounting pressures and continuing degradation. Defining a desired state for these habitats is a key step in implementing appropriate management but is often difficult given the challenges of available data and an evaluation of where to set benchmarks. We use more than 20 years of historical seagrass biomass data (1995-2018) for the diverse seagrass communities of Australia's Great Barrier Reef World Heritage Area (GBRWHA) to develop desired state benchmarks. Desired state for seagrass biomass was estimated for 25 of 36 previously defined seagrass communities with the remainder having insufficient data. Desired state varied by more than one order of magnitude between community types and was influenced by the mix of species in the communities and the range of environmental conditions. We identify a historical, decadal-scale cycle of decline with recovery to desired state in coastal intertidal communities. In contrast a number of the estuary and coastal subtidal communities have not recovered to desired state biomass. Understanding a historical context is critically important for setting benchmarks and making informed management decisions on the present state of seagrass in the GBRWHA. The approach we have developed is scalable for monitoring, management and assessment of pressures for other management areas and for other jurisdictions. Our results guide conservation planning through prioritization of the at-risk seagrass communities that are continuing to fall below their desired state.

A spatial analysis of seagrass habitat and community diversity in the Great Barrier Reef World Heritage Area.

The Great Barrier Reef World Heritage Area (GBRWHA) in north eastern Australia spans 2500 km of coastline and covers an area of ~ 350,000 km2. It includes one of the world's largest seagrass resources. To provide a foundation to monitor, establish trends and manage the protection of seagrass meadows in the GBRWHA we quantified potential seagrass community extent using six random forest models that include environmental data and seagrass sampling history. We identified 88,331 km2 of potential seagrass habitat in intertidal and subtidal areas: 1111 km2 in estuaries, 16,276 km2 in coastal areas, and 70,934 km2 in reef areas. Thirty-six seagrass community types were defined by species assemblages within these habitat types using multivariate regression tree models. We show that the structure, location and distribution of the seagrass communities is the result of complex environmental interactions. These environmental conditions include depth, tidal exposure, latitude, current speed, benthic light, proportion of mud in the sediment, water type, water temperature, salinity, and wind speed. Our analysis will underpin spatial planning, can be used in the design of monitoring programs to represent the diversity of seagrass communities and will facilitate our understanding of environmental risk to these habitats.

Connecting targets for catchment sediment loads to ecological outcomes for seagrass using multiple lines of evidence.

Catchment impacts on downstream ecosystems are difficult to quantify, but important for setting management targets. Here we compared 12 years of monitoring data of seagrass area and biomass in Cleveland Bay, northeast Australia, with discharge and associated sediment loads from nearby rivers. Seagrass biomass and area exhibited different trajectories in response to river inputs. River discharge was a slightly better predictor of seagrass indicators than total suspended solid (TSS) loads, indicating that catchment effects on seagrass are not restricted to sediment. Linear relationships between Burdekin River TSS loads delivered over 1-4 years and seagrass condition in Cleveland Bay generated Ecologically Relevant Targets (ERT) for catchment sediment inputs. Our predicted ERTs were comparable to those previously estimated using mechanistic models. This study highlights the challenges of linking catchment inputs to condition of downstream ecosystems, and the importance of integrating a variety of metrics and approaches to increase confidence in ERTs.

Current and future carbon stocks in coastal wetlands within the Great Barrier Reef catchments.

Australia's Great Barrier Reef (GBR) catchments include some of the world's most intact coastal wetlands comprising diverse mangrove, seagrass and tidal marsh ecosystems. Although these ecosystems are highly efficient at storing carbon in marine sediments, their soil organic carbon (SOC) stocks and the potential changes resulting from climate impacts, including sea level rise are not well understood. For the first time, we estimated SOC stocks and their drivers within the range of coastal wetlands of GBR catchments using boosted regression trees (i.e. a machine learning approach and ensemble method for modelling the relationship between response and explanatory variables) and identified the potential changes in future stocks due to sea level rise. We found levels of SOC stocks of mangrove and seagrass meadows have different drivers, with climatic variables such as temperature, rainfall and solar radiation, showing significant contributions in accounting for variation in SOC stocks in mangroves. In contrast, soil type accounted for most of the variability in seagrass meadows. Total SOC stock in the GBR catchments, including mangroves, seagrass meadows and tidal marshes, is approximately 137 Tg C, which represents 9%-13% of Australia's total SOC stock while encompassing only 4%-6% of the total extent of Australian coastal wetlands. In a global context, this could represent 0.5%-1.4% of global SOC stock. Our study suggests that landward migration due to projected sea level rise has the potential to enhance carbon accumulation with total carbon gains between 0.16 and 0.46 Tg C and provides an opportunity for future restoration to enhance blue carbon.

Climate drives the geography of marine consumption by changing predator communities.

The global distribution of primary production and consumption by humans (fisheries) is well-documented, but we have no map linking the central ecological process of consumption within food webs to temperature and other ecological drivers. Using standardized assays that span 105° of latitude on four continents, we show that rates of bait consumption by generalist predators in shallow marine ecosystems are tightly linked to both temperature and the composition of consumer assemblages. Unexpectedly, rates of consumption peaked at midlatitudes (25 to 35°) in both Northern and Southern Hemispheres across both seagrass and unvegetated sediment habitats. This pattern contrasts with terrestrial systems, where biotic interactions reportedly weaken away from the equator, but it parallels an emerging pattern of a subtropical peak in marine biodiversity. The higher consumption at midlatitudes was closely related to the type of consumers present, which explained rates of consumption better than consumer density, biomass, species diversity, or habitat. Indeed, the apparent effect of temperature on consumption was mostly driven by temperature-associated turnover in consumer community composition. Our findings reinforce the key influence of climate warming on altered species composition and highlight its implications for the functioning of Earth's ecosystems.

Green turtle (Chelonia mydas) grazing plot formation creates structural changes in a multi-species Great Barrier Reef seagrass meadow.

The Great Barrier Reef (GBR) contains extensive seagrass meadows with abundant and diverse herbivore populations. Typically, meadows in the region are multi-species and dominated by fast growing opportunistic seagrass species. However, we know little about how herbivores modify these types of seagrass meadows by grazing. We conducted the first megaherbivore exclusion study in the GBR at Green Island (Queensland) to understand how green turtle grazing structures these multi-species tropical seagrass meadows. After excluding green turtles for three months, we found that grazing only impacted seagrasses at one site, where green turtles created a grazing plot by actively feeding on both above and below ground seagrass structures, a rare observation for the species. Within this grazing plot at the end of the experiment, the un-caged control treatments open to grazing had a 60% reduction in both above and below ground biomass, and shoot height was reduced by 75%, but there was no impact of grazing on the seagrass species mix. Our study shows that grazing plot formation by green turtles occurs in GBR fast growing seagrass communities and reduces both above and below ground seagrass biomass, this behaviour may be targeting elevated leaf nutrients, or nutritional content of rhizomes. This study is the first documented case of grazing plot formation by green turtles in the GBR and suggests that grazing pressure has a major influence on seagrass meadow structure.

High variability of Blue Carbon storage in seagrass meadows at the estuary scale.

Seagrass meadows are considered important natural carbon sinks due to their capacity to store organic carbon (Corg) in sediments. However, the spatial heterogeneity of carbon storage in seagrass sediments needs to be better understood to improve accuracy of Blue Carbon assessments, particularly when strong gradients are present. We performed an intensive coring study within a sub-tropical estuary to assess the spatial variability in sedimentary Corg associated with seagrasses, and to identify the key factors promoting this variability. We found a strong spatial pattern within the estuary, from 52.16 mg Corg cm-3 in seagrass meadows in the upper parts, declining to 1.06 mg Corg cm-3 in seagrass meadows at the estuary mouth, despite a general gradient of increasing seagrass cover and seagrass habitat extent in the opposite direction. The sedimentary Corg underneath seagrass meadows came principally from allochthonous (non-seagrass) sources (~70-90 %), while the contribution of seagrasses was low (~10-30 %) throughout the entire estuary. Our results showed that Corg stored in sediments of seagrass meadows can be highly variable within an estuary, attributed largely to accumulation of fine sediments and inputs of allochthonous sources. Local features and the existence of spatial gradients must be considered in Blue Carbon estimates in coastal ecosystems.

Living at the margins - The response of deep-water seagrasses to light and temperature renders them susceptible to acute impacts.

Seagrasses inhabit environments where light varies at different timescales, nonetheless are acutely sensitive to reductions in light beyond some conditional bounds. Two tropical deep-water seagrasses, Halophila decipiens and Halophila spinulosa, from the Great Barrier Reef were tested for their response to defined light and temperature regimes to identify their growth requirements and potential thresholds of mortality. Species were exposed to two light intensities, saturating (75 µmol photons m-2 s-1) and limiting (25 µmol photons m-2 s-1) light and two temperature treatments (26 °C and 30 °C) over a four-week period. Wavelength-specific parameters of PSII photochemistry were evaluated for seagrass leaves, as well as shoot density, gas exchange, and pigment content. Both species were sustained under saturating light levels (3.2 mol photons m-2 d-1) while limiting light led to decreased shoot density for H. decipiens and H. spinulosa after two and four weeks, respectively. Wavelength-specific photochemistry was also affected under light-limiting treatments for both species while the functional absorption cross section was highly conserved. Photoacclimation and physiological adjustments by either species was not adequate to compensate for reduced irradiance suggesting these plants reside at the margins of their functional limits. As such, relatively short periods of light attenuating events, like dredging or flood plumes, may be detrimental to deep-water seagrass populations.

The Role of Herbivory in Structuring Tropical Seagrass Ecosystem Service Delivery.

Seagrass meadows support key ecosystem services, via provision of food directly for herbivores, and indirectly to their predators. The importance of herbivores in seagrass meadows has been well-documented, but the links between food webs and ecosystem services in seagrass meadows have not previously been made explicit. Herbivores interact with ecosystem services - including carbon sequestration, cultural values, and coastal protection. Interactions can be positive or negative and depend on a range of factors including the herbivore identity and the grazing type and intensity. There can be unintended consequences from management actions based on a poor understanding of trade-offs that occur with complex seagrass-herbivore interactions. Tropical seagrass meadows support a diversity of grazers spanning the meso-, macro-, and megaherbivore scales. We present a conceptual model to describe how multiple ecosystem services are influenced by herbivore pressure in tropical seagrass meadows. Our model suggests that a balanced ecosystem, incorporating both seagrass and herbivore diversity, is likely to sustain the broadest range of ecosystem services. Our framework suggests the pathway to achieve desired ecosystem services outcomes requires knowledge on four key areas: (1) how size classes of herbivores interact to structure seagrass; (2) desired community and management values; (3) seagrass responses to top-down and bottom-up controls; (4) the pathway from intermediate to final ecosystem services and human benefits. We suggest research should be directed to these areas. Herbivory is a major structuring influence in tropical seagrass systems and needs to be considered for effective management of these critical habitats and their services.

Contrasting impacts of light reduction on sediment biogeochemistry in deep- and shallow-water tropical seagrass assemblages (Green Island, Great Barrier Reef).

Seagrass meadows increasingly face reduced light availability as a consequence of coastal development, eutrophication, and climate-driven increases in rainfall leading to turbidity plumes. We examined the impact of reduced light on above-ground seagrass biomass and sediment biogeochemistry in tropical shallow- (∼2 m) and deep-water (∼17 m) seagrass meadows (Green Island, Australia). Artificial shading (transmitting ∼10-25% of incident solar irradiance) was applied to the shallow- and deep-water sites for up to two weeks. While above-ground biomass was unchanged, higher diffusive O2 uptake (DOU) rates, lower O2 penetration depths, and higher volume-specific O2 consumption (R) rates were found in seagrass-vegetated sediments as compared to adjacent bare sand (control) areas at the shallow-water sites. In contrast, deep-water sediment characteristics did not differ between bare sand and vegetated sites. At the vegetated shallow-water site, shading resulted in significantly lower hydrogen sulphide (H2S) levels in the sediment. No shading effects were found on sediment biogeochemistry at the deep-water site. Overall, our results show that the sediment biogeochemistry of shallow-water (Halodule uninervis, Syringodium isoetifolium, Cymodocea rotundata and C. serrulata) and deep-water (Halophila decipiens) seagrass meadows with different species differ in response to reduced light. The light-driven dynamics of the sediment biogeochemistry at the shallow-water site could suggest the presence of a microbial consortium, which might be stimulated by photosynthetically produced exudates from the seagrass, which becomes limited due to lower seagrass photosynthesis under shaded conditions.

Blue Carbon stocks of Great Barrier Reef deep-water seagrasses.

Shallow-water seagrasses capture and store globally significant quantities of organic carbon (OC), often referred to as 'Blue Carbon'; however, data are lacking on the importance of deep-water (greater than 15 m) seagrasses as Blue Carbon sinks. We compared OC stocks from deep-, mid- and shallow-water seagrasses at Lizard Island within the Great Barrier Reef (GBR) lagoon. We found deep-water seagrass ( Halophila species) contained similar levels of OC to shallow-water species (e.g. Halodule uninervis) (0.64 ± 0.08% and 0.9 ± 0.1 mg C cm-3, 0.87 ± 0.19% and 1.3 ± 0.3 mg C cm-3, respectively), despite being much sparser and smaller in stature. Deep-water seagrass sediments contained significantly higher levels (approx. ninefold) of OC than surrounding bare areas. Inorganic carbon (CaCO3) levels were relatively high in deep-water seagrass sediments (8.2 ± 0.4%) and, if precipitated from epiphytes within the meadow, could offset the potential CO2-sink capacity of these meadows. The δ13C signatures of sediment samples varied among depths and habitats (-10.9 and -17.0), reflecting contributions from autochthonous and allochthonous sources. If the OC stocks reported in this study are similar to deep-water Halophila meadows elsewhere within the GBR lagoon (total area 31 000 km2), then OC bound within this system is roughly estimated at 27.4 million tonnes.

Timing anthropogenic stressors to mitigate their impact on marine ecosystem resilience.

Better mitigation of anthropogenic stressors on marine ecosystems is urgently needed to address increasing biodiversity losses worldwide. We explore opportunities for stressor mitigation using whole-of-systems modelling of ecological resilience, accounting for complex interactions between stressors, their timing and duration, background environmental conditions and biological processes. We then search for ecological windows, times when stressors minimally impact ecological resilience, defined here as risk, recovery and resistance. We show for 28 globally distributed seagrass meadows that stressor scheduling that exploits ecological windows for dredging campaigns can achieve up to a fourfold reduction in recovery time and 35% reduction in extinction risk. Although the timing and length of windows vary among sites to some degree, global trends indicate favourable windows in autumn and winter. Our results demonstrate that resilience is dynamic with respect to space, time and stressors, varying most strongly with: (i) the life history of the seagrass genus and (ii) the duration and timing of the impacting stress.

Sediment Resuspension and Deposition on Seagrass Leaves Impedes Internal Plant Aeration and Promotes Phytotoxic H2S Intrusion.

HIGHLIGHTS: Sedimentation of fine sediment particles onto seagrass leaves severely hampers the plants' performance in both light and darkness, due to inadequate internal plant aeration and intrusion of phytotoxic H2S. Anthropogenic activities leading to sediment re-suspension can have adverse effects on adjacent seagrass meadows, owing to reduced light availability and the settling of suspended particles onto seagrass leaves potentially impeding gas exchange with the surrounding water. We used microsensors to determine O2 fluxes and diffusive boundary layer (DBL) thickness on leaves of the seagrass Zostera muelleri with and without fine sediment particles, and combined these laboratory measurements with in situ microsensor measurements of tissue O2 and H2S concentrations. Net photosynthesis rates in leaves with fine sediment particles were down to ~20% of controls without particles, and the compensation photon irradiance increased from a span of 20-53 to 109-145 µmol photons m-2 s-1. An ~2.5-fold thicker DBL around leaves with fine sediment particles impeded O2 influx into the leaves during darkness. In situ leaf meristematic O2 concentrations of plants exposed to fine sediment particles were lower than in control plants and exhibited long time periods of complete meristematic anoxia during night-time. Insufficient internal aeration resulted in H2S intrusion into the leaf meristematic tissues when exposed to sediment resuspension even at relatively high night-time water-column O2 concentrations. Fine sediment particles that settle on seagrass leaves thus negatively affect internal tissue aeration and thereby the plants' resilience against H2S intrusion.

Does Biodiversity-Ecosystem Function Literature Neglect Tropical Ecosystems?

Current evidence suggests that there is a positive relationship between biodiversity and ecosystem functioning, but few studies have addressed tropical ecosystems where the highest levels of biodiversity occur. We develop two hypotheses for the implications of generalizing from temperate studies to tropical ecosystems, and discuss the need for more tropical research.

Molecular physiology reveals ammonium uptake and related gene expression in the seagrass Zostera muelleri.

Seagrasses are important marine foundation species, which are presently threatened by coastal development and global change worldwide. The molecular mechanisms that drive seagrass responses to anthropogenic stresses, including elevated levels of nutrients such as ammonium, remains poorly understood. Despite the evidence that seagrasses can assimilate ammonium by using glutamine synthetase (GS)/glutamate synthase (glutamine-oxoglutarate amidotransferase or GOGAT) cycle, the regulation of this fundamental metabolic pathway has never been studied at the gene expression level in seagrasses so far. Here, we combine (i) reverse transcription quantitative real-time PCR (RT-qPCR) to measure expression of key genes involved in the GS/GOGAT cycle, and (ii) stable isotope labelling and mass spectrometry to investigate 15N-ammonium assimilation in the widespread Australian species Zostera muelleri subsp. capricorni (Z. muelleri). We demonstrate that exposure to a pulse of ammonium in seawater can induce changes in GS gene expression of Z. muelleri, and further correlate these changes in gene expression with 15N-ammonium uptake rate in above- and below-ground tissue.